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Heterodox Concepts in Modern Evolutionary Embryology, 1900-1950 Andres Galera* Centro de Ciencias Humanas y Sociales, IH, CSIC, Spain.

*Corresponding author. Tel: (+34) 916022462; E-mail: [email protected] Citation: Galera A. Heterodox Concepts in Modern Evolutionary Embryology, 1900-1950. Electronic J Biol, 12:4 Received: May 31, 2016; Accepted: June 24, 2016; Published: July 01, 2016 Review Article

embryogenesis as a telling of the evolutionary Abstract history of a species, exploded, under different titles, during the early 1800s. The theory soon became Whatever the evolutionary model we adopt, in the part of embryological knowledge, but its strongest case of sexual reproduction, the process has an involvement in the evolutionary debate took place in embryological significance because this is the way the 1860s. It is well known that most of the credit to generate individuals and to perpetuate the life. belongs to the German zoologist Ernst Haeckel and The connection between evolution and embryology his book Generelle Morphologie der Organismen, is a necessary event. In this evolutionary context, the published in 1866 [1]. Known as the biogenetic law, key question is: how two species are formed from Haeckel’s theory states that the different embryonic the same biological unit? During the first half of the states represent the different adult forms adopted 20th century embryologists as Richard Goldschmidt, by the species along its evolutionary path. In brief, Conrad Waddington, and Walter Garstang answered ontogeny recapitulates phylogeny. This statement the question from a heterodox point of view. They is as widespread as it is erroneous. Let us take the introduced new concepts that changed the way case of the human species. During its development, to thinking the evolution. This essay analyzes this the human embryo resembles, successively, a fish, unorthodox thought and its scientific impact. an amphibian, a reptile, a mammal, a primate, until finally adopting the human morphology. Keywords: Epigenetic landscape; Evolution; Embryology; Garstang; Goldschmidt; Heterochrony; Under recapitulation theory, evolution is a summary Hopeful monster; Mendelian heredity; Recapitulation; of parts, each identifying a specific final product. Let Waddington. us ask ourselves, how does this happen? Haeckel divided inheritance into two categories. One group Introduction contained standard characteristics transmitted by Taking things to the simplest level, we can say that the parents. The second consisted of characteristics the fundamental problem of organic evolution knows acquired by the adult through adaptation to its how a living being is formed. Multi-cellular organisms environment. This was a unique concession to habitually use sexual reproduction to multiply: the Lamarck. Acquired inheritance was the source of fusion of parental gametes makes up a cell with evolutional variability, manifested in the final phase of the potential to develop into another individual. Our the embryonic cycle and thus increasing the number analysis will focus on this mode of reproduction. In of stages. Under evaluation, the argument presents sexual reproduction, evolution takes place when a serious practical problem that did not go unnoticed. information regarding morphological changes is The continuous addition of evolutionary stages integrated into the reproductive mechanism. The would result in a physiological distortion of ontogeny, connection between evolution and embryology is making it unfathomable. The biogenetic law was clear – it is a necessary occurrence. Embryologists therefore reformulated. Embryogenesis would no swiftly made this connection, back in the 19th century, longer constitute an absolute recapitulation, but a th when the theory of evolution was first formulated. condensed repetition of a species’ past. By the 20 Under this criterion, the question of how species century there was little doubt as to the falsehood of evolve is directly linked to embryogenesis. The the theory. Haeckel himself acknowledged having purpose is to understand how a new species is manipulated tests in order to facilitate comprehension, formed during the morphological sequence occurring by simulating a common evolutionary sequence in the ovum after fertilisation. In order to achieve this, between the embryos of the different species he it became necessary to understand the mechanisms had compared [2-4]. Embryology returned to the that control the reproductive process. scientific logic expressed by the biologist Ernst von Baer in the 1820s. A simple, common sense Supported by compared embryology, the theory of argument: the embryo only resembles members recapitulation, i.e., the conception of considering of its own species, and over the course of its

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development progresses from a general state to The idea was to explore whether progeny displayed a particular state, from amorphous to specific, the spontaneous modifications established under gradually acquiring the anatomical characteristics the theory. This objective was partly achieved. After of the informative being contained in the ovum [5]. a number of years, an individual with white eyes Embryonic coincidences between different groups was born. This fly proved the existence of natural are no more than a reflection of their common past. mutations, although its evolutionary significance was An embryo does not recapitulate its past; it partially not as had been expected: it was not a new species repeats the ontogeny of its ancestors. So, what is the of fly. Tens of experimental mutants would appear evolutionary significance of reproduction? This is a over the following years. Flies with no wings, or with relevant, necessary and cardinal matter, shaped over their wings curled up, stunted or grooved, and flies the course of the 20th century via genetics and the with brown, chestnut or peach-coloured eyes, are biology of development. examples of this amazing zoology resulting from genetic manipulation. With this glimpse into the An early answer to the question was obtained modus operandi of the genome, some of pieces of in 1866, although it went unnoticed. This is the the morphogenetic puzzle began to fall into place: notorious pea plant experiment carried out by Gregor the chromosome is the material container of the Johann Mendel at the Cistercian Abbey in Brno. gene, the expression of which regulates embryonic Over the course of a decade this monk crossbred differentiation. Published in 1915, The Mechanism thousands of plants and examined their fruit. He of Mendelian Heredity contained the results of this studied their shape, size, colour and texture in order work. The book established the foundations of to explain evolution in a precise context: discovering modern genetics [9]. what biological mechanism enables offspring to inherit parental traits. His hereditary theory laid Under the denomination synthetic theory or modern the foundations for genetics. In his mind, species synthesis, Neo-Darwinism easily assimilated the did not evolve either under the influence of their pattern of gene variation by applying a well-known environment or guided by natural selection. Chance recipe: cause and effect [10]. It was thought that was responsible for mixing parental characteristics evolution was an exact science written in a genetic during fertilisation. Spontaneously at times, the language. Evolution would have an exclusively resulting genetic combination would stabilise in the genic medium resulting from the expression of small offspring. In this case, descendants would suddenly mutations, causing occasional modifications in form a specific, reproductively constant group. population typology – the group in which selection Another species would emerge. Plainly speaking, takes place. Repeated on a gradual, ongoing and evolution would be the consequence of a singular accumulative basis, the phenomenon would explain chromosomic recombination [6]. how species diversify over time via the gradual and selective addition of mutations. Population genetics In 1900, Mendel’s laws were rediscovered, and would characterise Neo-Darwinism for decades. genetics started its unstoppable biological ascent. First there was the formulation of chromosomic theory; Hopeful monsters then came the notion of genes: the chromosomic unity responsible for phenotypical expression. From 1880 onwards, embryology was a purely Using Mendel’s model, the Dutch botanist Hugo de experimental discipline that had broken the bounds of Vries, one of the fortunate rediscoverers, wrote Die descriptive procedure. The mechanics of embryonic mutationstheorie; two innovative volumes devoted to development were under investigation. Many the origin of species [7,8]. In summary, his mutation questions arose. The main question to be answered theory ventured that evolution did not follow Darwin’s was how cellular, tissue, and organic differentiation principles. Species were not formed via the slow, influenced the construction of the individual. This gradual accumulation of small organic changes, but biological problem focused on discovering what through the reproductive manifestation of abrupt factors determined the transformation of the embryo. typological variations, spontaneous, stable, sudden, Research progressed towards the definition of hereditary changes, known as mutations, that the event as a chain reaction, meaning that the immediately altered the parental typology. This event organisational structure induced in one stage would would be collective and final; occurring in different be a triggering factor for the next, and so on. Next morphological groups of descendants. Mutation came the concept of the morphogenetic field: the replaced natural selection as the presumed motor embryo is organised into self-regulating areas, behind evolution. It would now be the primary cause. called fields, each acting to create a certain type of anatomy. These fields are correlatively adapted Only a few years later, convinced by Mendelism, to the embryological stage, governing what take the embryologist Thomas Hunt Morgan, of the place at all times. This means that the process University of Columbia, started his experiments with has the necessary plasticity to reach the relevant Drosophila melanogaster, better known as the fruit organisational level for each successive stage. fly. This tiny, hairy insect with protruding, vermillion- This was the 1920s, 1930s and 1940s. Adding up coloured eyes was to revolutionise genetics. In all genetic theory, the embryological model was the Morgan’s laboratory, flies were not bred by chance. product of a complicated physiological process of a

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genic origin; but the assumed equivalence between University of Friburg, and his student Hilde Mangold, the genome and morphology was insufficient to published the results of their experiments with newt explain to interactive embryonic framework. At this embryos, showing embryonic induction; a milestone point, upon identifying evolution as a mutational in developmental biology. It is an easy concept phenomenon, biologists asked themselves, how to explain; the difficulty lies in establishing how it does genomic change affect ontogeny by tracing happens. Early on in its development, after the stage out new life? The challenge was to develop a unified known as gastrulation, an embryo differentiates an theory that could integrate cellular chromosomic area of tissue that takes control of embryogenesis, information with the embryological process triggered determining its future organisation. It is known as by fertilisation. Richard Goldschmidt, an unorthodox the organiser, characterised by its multifunctional German geneticist residing in the United States, validity: when a section of this tissue is grafted onto a professor at the University of Berkley from another embryo, this second organiser generates a 1936, accepted the challenge. He addressed the secondary embryo using the cellular structure of the issue openly, head on. His theory was published recipient. The developmental schedule is executed in 1940, in a book called The Material Basis of through chemical signals. Over sixty years would go Evolution [11]. This manual contained four hundred by before we understood the molecular basis of this pages devoted to the consolidation of a bifocal mechanism. embryogenetic outline, based on the concepts of macro and microevolution. The general hypothesis Embryonic induction was the path taken by the regarded evolution as an embryological event, with British naturalist Conrad Hal Waddington as he chromosomes as the fundamental ingredient. Two traced the supposed synthesis between embryology, mechanisms would act to re-design populations. One genetics and evolution. The correct question was: was microevolution, the result of the appearance How can the informative rigidity of the genetic of micro mutations, identified as morphological code, the conservational nature of the ontogenic alterations in line with the anatomical structure of the system and evolutionary variability be compatible? species and, therefore, compatible with the existing During the 1930s Waddington investigated the embryonic schedule. This change would involve the subject in mammals and birds. He carried out some adaptive improvement of a group to a specific region surprising experiments. One of the most famous of within the distribution area of that species, creating these was the transplantation of a rabbit organiser sub-species, breeds or varieties. Simply put, without into a chicken embryo, causing the formation of a losing identity, typology is efficiently reshaped in order standard secondary embryo. If nothing else, the to inhabit local environments. Micro mutation would inter-special nature of the experiment proved that be an evolutionary dead end; it would constitute a the signal emitted by the organiser is the same in mechanism of specialisation incapable of producing different species of vertebrates. The response does new species. not depend on the composition of genes, but on their expression. There are of course genetic differences, However, evolution is synonymous with and molecular similarities, chemical markers that macroevolution. This notion is defined as a genomic are recognisable to the cellular unit regardless of reorganisation – called systemic mutation – to a the origin of the organic matter. This is information degree that constitutes a new chromosomic pattern; regarding the activation of the process, never another genetic system. The emergence of a different on the content of the morphological programme, information system would also lead to a different which remains unaffected. Waddington’s solution ontogenic process. This change would be the origin defined the activity of the organiser as a more of new organisms belonging to a new evolutionary complex event than a mere response to a signal. line, viable provided they find an environmental niche Let us simplify. Waddington proposed that the suited to their innovative nature. The first bird hatched genes in question, known as homeotic genes, have from a reptile’s egg, explained Goldschmidt to illustrate a quantitative effect and act together. The chemical the idea. This was the hopeful monster: the embryonic markers resulting from genetic transcription establish formation of anomalous beings, preadapted to a concentration gradients, behaving like beacons different environment. Evolution would take place that channel the spatial distribution of cells and as a succession of evolutionary leaps in disharmony thereby the morphological identity to be constituted with the gradual-selective pattern established under subsequently. The outline is known as the epigenetic synthetic theory. Given his rebelliousness and landscape, an intuitive ontogenic scenario where the different way of thinking, the German scientist was set of cells is guided by chemical signals towards the ignored, condemned, ridiculed and excluded from different paths that they need to follow. What is the evolutionist thought [12]. However, the validity of his evolutionary purpose of this model? The fundamental proposal is being reconsidered as it explains certain intention is to integrate genetics and evolution as evolutionary episodes, for example as a formula for elements in a dynamic system, and place them at the speciesisation of the botanical group of the orchids. different operational levels in order to prevent the introduction of evolutionary changes from causing a Epigenetic landscape chromosomic reorganisation incompatible with the viability of the organism. The concept of the epigenetic In 1924, Hans Spemann, professor of zoology at the landscape associates the variability of an alteration

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of genetic expression with a full or partial inhibition of evolutionary significance by investigating the life gene function, causing a different cellular response cycle of the ascidia. This colourful tunicate, tube and leading to a different typology. Simultaneously, shaped and fragile-looking, populates the seabed this system’s unique structure allows it to interact after maturing. However, its young proliferate with the external environment, making it viable to freely in the ocean, propelled by an unusual caudal inherit acquired characteristics. Conrad Waddington appendix. This strange tail bears a dorsal thread was one of the great 20th century theorists on known as the notochord. This solid cellular rod developmental embryology and evolution. He was resembles an incipient backbone, and disappears an indisputable reference point, even beyond the upon maturing into adulthood. The notochord is 1950s. Organizers and genes, and The strategy of one of the distinctive evolutionary characteristics the genes, were fundamental pieces of work in this –synapomorphies– of chordates; a group primarily field [13,14]. consisting of vertebrates. This fact led Garstang to identify the evolutional origin of the group as an Heterochrony invertebrate ancestor with a larval development similar to that of the ascidia. At some point, under Ontogeny does not recapitulate Phylogeny: it specific circumstances, the juvenile acquired creates it. This statement was made by the British reproductive ability, maintaining the dorsal chord as zoologist Walter Garstang. It was published in a fundamental part of its anatomy. These specimens 1922, in his article The theory of recapitulation: would be the seed for a successful evolutionary line a critical re-statement of the biogenetic law [15]. that went on to adopt thousands of different shapes. Eight words, just eight, were enough to refute With his investigation, Garstang opened a genuine the theory. These words were necessary in order embryological window on evolution, which until that to interpret evolution by applying a revolutionary time had been unthinkable [16]. His contemporary embryological criterion. Which one? The idea was British embryologist, Gavin de Beer, took up this simple, ingenious, and possible. The idea required opportunity. However, it would be the palaeontologist a conceptual turnaround to alter the order of Stephen Jay Gould who would make the argument things; necessary in order to ensure that the result an evolutionary benchmark during the last quarter of reproduction is an end product different to that of the 20th century. His work Ontogeny & phylogeny, established in the chromosomes. The strategy published in 1977, is a classic in biological sciences consisted of following the path of evolution using [17]. Today, this innovative way of thinking makes the juvenile ontogenic forms. A specialist in marine up a substantial part of evolutionary developmental invertebrates, Garstang detected the evolutionary biology, better known as evo-devo. implications of the approach taken to external sexual reproduction; widespread in this zoological group. Conclusion Fertilisation takes place in the water. The fertilised egg gives way to a sequential larva transformation At this point, it is essential to stress that that shapes the individual until it becomes an evolutionary embryology highlights learning about adult. Each stage in this life cycle represents a and deconstructing the reproductive process, self-sufficient organic outlie, differentiated from the and understanding how the system changes spontaneously to generate different organisms. adult in its anatomical composition and reproductive The action occurs because of a structurally defined immaturity. Here we find the heart of the matter. situation, a circumstance that affects the process. Why? We could categorise the larva stage as a Evolution does not have a metaphorical free hand. potential hopeful monster adapted to the medium Our presentation ended in the mid-20th century. The of water that, incapable of independent living, story is not yet complete. The second half of the continues the routine metamorphosis indicated on century presented interesting new developments. the embryonic script. Considering the typological Of particular note was the approach developed separation found in adults, in order to create a new by the French embryologist Rosine Chandebois species it would be sufficient for juveniles to acquire in the early 1980s. Her theory is an anti-Darwinist the ability to reproduce prematurely. All this takes evolutionary proposal, the purpose of which is to place across a time-space alteration. The process build up a new logic of the living being. How can is direct, immediate and conservative – it does this be achieved? By referring to the similarities not require new structures to be created-, decisive in comparing the major lines of evolution with the characteristics for determining viability. This was the general parameters traced by the developing embryo pattern proposed by Walter Garstang: considering [18]. But that is not our story to tell today. Finally, we the potency of juvenile states for manifesting a new must remember that the solution to the evolutionary evolutionary line. The conclusion was that ontogeny puzzle is complex but not unique. There are still creates phylogeny. Early sexual maturity occurs many pieces to be discovered. Of the ones we know when there is an alteration in ontogenic synchronism about, some are in the wrong place, and others we (heterochrony): the development of the gonads is haven’t found a place for yet. Patience, tenacity brought forward, allowing incomplete specimens and open-mindedness are the qualities required to to reproduce – the axolotl is an existing example progress in the biological process of understanding of this phenomenon. Garstang’s model took on full the past present future of life.

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